Open access peer-reviewed chapter - ONLINE FIRST

Use of Shear Wave Elastography in Pediatric Musculoskeletal Disorders

Written By

Celik Halil Ibrahim and Karaduman Aynur Ayşe

Submitted: December 11th, 2021Reviewed: December 16th, 2021Published: January 16th, 2022

DOI: 10.5772/intechopen.102063

IntechOpen
Elastography - Applications in Clinical MedicineEdited by Dana Stoian

From the Edited Volume

Elastography - Applications in Clinical Medicine [Working Title]

Dr. Dana I Stoian and Dr. Alina Popescu

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Abstract

Muscle shear-wave elastography (SWE) is an exciting and rapidly evolving ultrasound technique that allows quantification of muscle stiffness with a non-invasive, non-painful and non-irradiating examination. It has the potential of wider clinical use due to relatively low-cost, providing real-time measurement and, especially for the pediatric population, taking less time and sedation/anesthesia-free. Research indicate that muscle SWE shows promise as an adjunct clinical tool for differentiating between a normal and an abnormal muscle, monitoring the effectiveness of therapeutic interventions, altering the therapeutic intervention, or deciding treatment duration. This chapter will aim to provide an overview of the knowledge about the using of muscle SWE in common pediatric musculoskeletal disorders such as Duchenne Muscular Dystrophy, Cerebral Palsy, Adolescent Idiopathic Scoliosis, and Congenital Muscular Torticollis in the light of current evidence.

Keywords

  • shear-wave elastography
  • ultrasound elastography
  • muscle stiffness
  • muscle elasticity
  • musculoskeletal disorders

1. Introduction

Palpation is an ancient diagnostic method that has been used in medical practice for thousands of years since Hippocrates’ day. Nevertheless, palpation is still valuable and often preferred today to assess the mechanical properties of a tissue in many clinical settings. However, some disadvantages such as limited tissue accessibility and inherent subjectivity may cause hesitations in its use [1]. To overcome these disadvantages by providing a more objective assessment of tissue mechanical properties, Magnetic Resonance Imaging Elastography and Ultrasound Elastography (USE) are the options offered by today’s technology. However, the latter has the potential for wider clinical use because it is relatively low-cost, it provides real-time measurement, it takes less time, especially for the pediatric population, and it is sedation/anesthesia-free. The rapidly evolving evidence appears to be very promising that USE may be used to assess the mechanical properties of a tissue, especially muscle stiffness, that is, the degree of muscle resistance to deformation [2, 3, 4].

To briefly explain the basic principle, USE measures deformation in response to force/stress applied to the muscle. There are various USE techniques (strain elastography, Acoustic radiation force impulse [ARFI], Transient elastography, and Shear-wave elastography [SWE]), depending on the way of stress application and the measurement of deformation. SWE quantitatively measures muscle stiffness based on shear-wave propagation within the tissue and seems to be ahead of other USE techniques due to some prominent features such as less user-dependency, providing quantitative results besides elastogram, and higher reliability and repeatability [1, 4].

SWE shows promise as an adjunct clinical tool for differentiating between a normal and an abnormal muscle, monitoring the effectiveness of therapeutic interventions, altering the therapeutic intervention, or deciding treatment duration. Therefore, SWE, which measures individual muscle stiffness, can provide significant benefits, especially for physiotherapists because many rehabilitation strategies aim to change the muscle structure.

This chapter aims to present an overview of the knowledge about the use of muscle SWE in common pediatric musculoskeletal disorders such as Duchenne Muscular Dystrophy and Adolescent Idiopathic Scoliosis in the light of current evidence.

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2. Shear-wave elastography in pediatric musculoskeletal disorders

2.1 Duchenne muscular dystrophy

Duchenne Muscular Dystrophy (DMD), which is the most common childhood neuromuscular disease with a prevalence of 1/3600–9300, is an X-linked recessive hereditary disease characterized by progressive muscle degeneration and weakness [5, 6]. The natural course of DMD includes pathological muscle changes, including a decrease in the number of normal muscle cells, dystrophic changes in myofibrils, and the replacement of normal muscle cells by adipose and fibrous tissues [7].

It is difficult to evaluate pathological changes in muscles and ultimately disease progression in patients with DMD because repeated muscle biopsies are invasive and not easily obtained [8, 9]. Therefore, it is emphasized that there is a need for reliable and non-invasive objective assessment tools that can be used routinely to evaluate disease progression and the efficacy of therapeutic interventions [10]. In response to this need, it has been emphasized in recent years that SWE is a promising clinical assessment tool to evaluate muscle pathology and disease progression in DMD [10, 11, 12, 13].

Lacourpaille et al. and Pichiecchio et al. have found that lower and upper extremity muscle stiffness was higher in children with DMD compared with healthy controls and that SWE was able to distinguish between normal and dystrophic muscles [11, 12]. In another study, it was shown that muscle stiffness increased significantly in children with DMD after a 12-month follow-up period while muscle stiffness was stable in controls, and it was stated that SWE has the potential to be used in monitoring DMD progression [13]. Lin et al. reported that the stiffness of the tibialis anterior and the gastrocnemius medialis muscles decreased from ambulatory to early non-ambulatory stages, whereas the stiffness of the rectus femoris muscle increased. This result pointed out that individual muscles have different alteration patterns in stiffness as the ambulatory function declined and that SWE may be useful in the classification and prediction of ambulation status in children with DMD [10]. Additional information on muscle SWE studies in children with DMD is provided in Tables 1 and 2.

AuthorsParticipantsMusclesFindings
Lacourpaille [12]14 children with DMD (age: 13.3 ± 5.9 y); 13 healthy controls (age: 12.8 ± 5.5 y)TA, GM, VL, BB, TB, ADMSignificantly higher muscle stiffness in DMD patients compared with controls for all muscles, except for ADM.
Lacourpaille [13]10 children with DMD (age range: 7–22 y); 9 healthy controls (age range: 7–22 y)TA, GM, BB, TB, ADMSignificant increase in TA, GM, and TB stiffness over 12 months follow-up in patients with DMD while stiffness was stable in controls.
Pichiecchio [11]5 preschool children with DMD (age range: 3.2–4.9 y); 5 healthy controls (age range: 3.3–3.9 y)GM, RF, VM, VL, AM, TA, GMaxMuscle stiffness of the DMD patients was moderately higher than controls in the RF, VL, AM, and GMax muscles, whereas VM, TA and GM muscles of DMD patients were only minimally more stiff.
Lin [10]39 children with DMD (age: 10.4 ± 3.8 y); 36 healthy controls (age: 9.2 ± 4.1 y)RF, TA, GMThe stiffness of the RF and GM muscles was significantly higher in DMD patients compared with the control group.
The stiffness of the TA and GM muscles decreased from ambulatory to early non-ambulatory stages, whereas the stiffness of the RF muscle increased from ambulatory to late non-ambulatory stages in DMD patients.

Table 1.

Studies using muscle shear-wave elastography in Duchenne muscular dystrophy.

GMax, gluteus maximus; AM, adductor magnus; ADM, abductor digiti minimi; BB, biceps brachii; GM, gastrocnemius medialis; GL, gastrocnemius lateralis; RA, rectus abdominis; RF, rectus femoris; TA, tibialis anterior; TB, triceps brachii; VL, vastus lateralis; VM, vastus medialis.

MusclesLacourpaille 2015 [12]Pichiecchio 2018 [11]Lin 2021 [10]
TADMD23.1 ± 14.7 kPa11.64 ± 1.35 kPa2.87 ± 0.77 m/s
HC12.5 ± 3.1 kPa13.54 ± 3.99 kPa2.70 ± 0.42 m/s
GMDMD21.9 ± 12.7 kPa12.9 ± 3.45 kPa2.19 ± 0.57 m/s
HC14.5 ± 3.5 kPa12.18 ± 5.56 kPa1.85 ± 0.28 m/s
VLDMD21.5 ± 18.8 kPa14.26 ± 1.34 kPa
HC9.6 ± 2.2 kPa7.8 ± 2.74 kPa
VMDMD15.30 ± 2.43 kPa
HC11.56 ± 3.29 kPa
RFDMD14.44 ± 2.64 kPa2.10 ± 0.72 m/s
HC8.10 ± 1.19 kPa1.77 ± 0.28 m/s
GMaxDMD13.92 ± 2.76 kPa
HC9.92 ± 1.31 kPa
AMDMD14.10 ± 1.31 kPa
HC9.74 ± 3.09 kPa
BBDMD34.9 ± 23.3 kPa
HC18.9 ± 6.4 kPa
TBDMD8.7 ± 2.1 kPa
HC7.3 ± 1.4 kPa
ADMDMD14.1 ± 7.8 kPa
HC11.9 ± 5.0 kPa

Table 2.

Muscles stiffness values in Duchenne Muscular Dystrophy.

2.2 Cerebral palsy

Cerebral palsy (CP), a neurodevelopmental disorder caused by non-progressive immature brain disturbances, affects 2.11 of every 1000 children in high-income countries and is often considered to be the most common childhood motor disability [14, 15]. In CP, spasticity caused by an upper motor neuron lesion often leads to muscle weakness, muscle stiffness, and contractures, which eventually restrict general mobility [16]. Recent studies have emphasized the increased intensity of the connective tissue and extracellular matrix in spastic muscles, indicating that muscle stiffness may be a critical factor in the worsening of motor disorder over time in children with CP [17, 18]. These research findings may explain our clinical observations that many children with CP have an increase in muscle stiffness and a decrease in joint range of motion and in the efficiency of walking as they age into adolescence and adulthood. Therefore, it is not surprising that many studies have evaluated muscle stiffness with SWE in children with CP.

Muscle SWE studies comparing healthy children and children with CP have reported that muscle (GM, GL, BB, and SoL) stiffness is significantly higher in children with CP [16, 19, 20, 21]. Lee et al. [22] and Boulard et al. [23] have noted that muscle stiffness was higher in the more-affected limb than in the less-affected limb of children with CP. In addition, positive correlation has been reported between muscle stiffness and spasticity [20, 24, 25]. SWE has been used not only to distinguish between spastic and normal muscles but also to evaluate intervention effectiveness. All but one [26] of the studies investigating the effectiveness of botulinum toxin A (BTX) injection have reported a significant decrease in muscle stiffness a month after the injection [24, 25, 27]. In addition, it was stated that muscle stiffness values after 3 months is not significantly different from baseline values due to the duration of the effect of botulinum toxin [26]. In a study examining the relationship between hip muscle stiffness and hip dislocation, it was reported that there was a correlation between the Reimers Migration Index and the stiffness of the adductor magnus and the iliopsoas muscles [28]. Additional information on muscle SWE studies in children with CP is provided in Tables 3 and 4.

AuthorsParticipantsMuscle(s) and Stiffness ValuesFindings
Lallemant-Dudek [19]16 children with CP (age: 8.3 ± 2.8 y); 29 healthy controls (age: 12.1 ± 3.3 y)GMBBIntra-rater ICC: 0.90 and inter-rater ICC: 0.92 in healthy controls.
Stretched GM was significantly stiffer in CP than in controls. GM at rest did not show any difference between groups, nor did BB either at rest nor stretched.
Stretched GCM; CP: 8.8 ± 4.1 m/s
Controls: 2.9 ± 0.7 m/s
GCM at rest
CP: 3.1 ± 1.8 m/s
Controls:1.8 ± 0.6 m/s
did not provide original data
Vola [20]21 children with CP (age range: 3–16 y); 21 healthy controls (age range: 3–14 y)SoL
CP: 8.1 ± 2.3 kPa
Controls: 4.8 ± 1.7 kPa
Muscle stiffness is significantly higher in children with CP compared with controls. High positive correlation (r = 0.74) between muscle stiffness and spasticity (MAS).
Lee [22]8 children with CP (age: 9.4 ± 3.7 y)GM
more affected: 5.05 ± 0.55 m/s, less-affected: 4.46 ± 0.57 m/s
TA
more affected:
3.86 ± 0.79 m/s, less-affected: 3.22 ± 0.40 m/s
Muscle stiffness of the GM and TA in the more-affected limb was higher than in the less-affected limb.
Brandenburg [16]13 children with CP (age range: 2–12 y); 13 healthy controls (age range: 2–12 y)GL
CP: 15.0 (11.6, 17.5) kPa
Controls: 7.8 (6.1, 11.0) kPa
Muscle stiffness is significantly higher in children with CP compared with controls.
Boulard [23]11 children with CP (age: 11.1 ± 1.7 y)GM
more-affected: 10.2 ± 2.6 kPa
less-affected: 7.9 ± 1.5 kPa
Muscle stiffness of the stretched GM in the more-affected limb was higher than in the less-affected limb.
Bilgici [21]17 children with CP (age: 9.25 ± 2.68 y); 25 healthy controls (age: 10.40 ± 2.76 y)GM
CP: 3.17 ± 0.81 m/s
Controls: 1.45 ± 0.25 m/s
Muscle stiffness is significantly higher in children with CP compared with controls.
Doruk Analan [28]25 children with CP (age: 4.07 ± 2.25 y);AM, IP
AM: 2.65 ± 1.03 m/s
IP: 2.61 ± 0.85 m/s
AM and IP muscle stiffness show correlation with the Reimers Migration Index (0.70 and 0.71, respectively).

Table 3.

Studies using muscle shear-wave elastography in cerebral palsy-1.

IP, Iliopsoas; AM, adductor magnus; BB, biceps brachii; GM, gastrocnemius medialis; GL, gastrocnemius lateralis; SoL, Soleus; TA, tibialis anterior; MAS, Modified Ashworth Scale; kPa, kilopascal.

AuthorsParticipantsMuscle(s) and Stiffness ValuesFindings
Bilgici [24]12 children with CP (age: 8.58 ± 2.48 y);GM
Before: 3.20 ± 0.14 m/s
After: 2.45 ± 0.21 m/s
Significant decrease in muscle stiffness a month after BTX injection.
Muscle stiffness is correlate with MAS (r = 0.578).
Brandenburg [26]10 children with CP (age range: 2.1–8.8 y);GL
(The article provided the change values, not the original values.)
Notable, but non-significant, decrease in muscle stiffness 1 month after BTX injection.
Baseline muscle stiffness is not significantly different from 3 month after BTX injection.
Bertan [27]17 children with CP (age: 4.6 ± 1.2 y); 16 children with CP (Control group) (age: 4.4 ± 1.2 y)GMGLSignificant decrease in muscle stiffness of GM and GL 1 month after BTX injection in study group while no significant decrease in the control group.
Before and after values for CP: 2.32 ± 0.50 and
2.08 ± 0.47 m/s
Before and after values for controls:
2.34 ± 0.53 and
2.32 ± 0.48 m/s
Before and after values for CP: 2.07 ± 0.37 and 1.90 ± 0.31 m/s
Before and after values for CP: 2.10 ± 0.48 and 1.98 ± 0.40 m/s
Dağ [25]24 children with CP (age: 6 ± 2.8 y);GM
Before: 45.9 ± 6.5 kPa
After: 25.0 ± 5.7 kPa
Significant decrease in muscle stiffness 1 month after BTX injection.
Muscle stiffness is correlate with MAS and MTS (r = 0.77 and 0.79, respectively).

Table 4.

Studies using muscle shear-wave elastography in cerebral palsy-2.

GM, gastrocnemius medialis; GL, gastrocnemius lateralis; MAS, Modified Ashworth Scale; MTS, Modified Tardieu Scale; BTX, botulinum toxin; kPa, kilopascal.

2.3 Adolescent idiopathic scoliosis

Adolescent idiopathic scoliosis (AIS), the most common type of scoliosis, is a 3D spinal deformity characterized by the deviation of the spine in the sagittal, frontal, and transverse plane [29]. The etiology of AIS has remained unclear until today even though many hypotheses have been put forward to explain the origin of this deformity [30].

Asymmetric loading on the vertebrae may be one of the causes contributing to the etiology of AIS [31]. Therefore, studies evaluating muscle stiffness with SWE and investigating muscle imbalance have been conducted to clarify the etiology of scoliosis. It has been suggested that this asymmetrical load may be caused by the paravertebral and lateral abdominal muscles consisting of the transversus abdominis (TrA), obliquus internal (OI), and obliquus external (OE) [32, 33]. Liu et al. reported no significant difference in paravertebral muscle stiffness between the concave and the convex side of scoliosis [32]. In a study examining the stiffness of the lateral abdominal muscles (TrA, OI, and OE), it was stated that there were no differences between healthy control and AIS groups in terms of muscles stiffness at rest and during isometric contraction and also there was no muscles stiffness asymmetry between the concave and the convex sides of scoliosis [33]. In addition, the same research group found that stiffness measurements of the lateral abdominal muscles were carried out with high reliability/agreement during contraction, while the reliability of the stiffness measurements ranged from moderate to excellent at rest [34]. Another issue that attracts the attention of researchers is the involvement of respiratory muscles in scoliosis. By altering the biomechanics of the rib cage, scoliosis can affect the intercostal muscles (ICMs), thoracic expansion, and ultimately respiration. However, Pietton et al. investigated the stiffness of the ICMs in healthy control and AIS groups and reported that there was no significant difference between groups, although the AIS group displayed a trend toward higher stiffness of the ICMs than in the healthy group [35]. Additional information on muscle SWE studies in children with CP is provided in Table 5.

AuthorsParticipantsMuscle(s) and stiffness valuesFindings
Linek [34]35 children and adolescents with AIS (age: 12.8 ± 2.8 y)OE, OI, TrA
OE:21.1 ± 9.19 kPa
OI:14.6 ± 4.24 kPa
TrA:13.8 ± 4.22 kPa
At rest, the reliability of stiffness measurements ranged from moderate to excellent in all examined muscles (ICC: 0.56–0.94).
During contraction, muscles stiffness was measured with high reliability/agreement (ICC:0.63–0.91).
Linek [33]108 children and adolescents with AIS (age range: 10–17 y); 151 healthy controls (age range: 10–17 y)OE, OI, TrA
For AIS;
OE:16.6 ± 5.64 kPa
OI:15.5 ± 4.63 kPa TrA:14.1 ± 3.50 kPa
For healthy
controls;
OE:16.2 ± 5.67 kPa
OI:15.2 ± 4.03 kPa
TrA:13.9 ± 3.06 kPa
There were no differences between control and AIS groups in the muscles stiffness at rest and during isometric contraction.
There were no muscles stiffness asymmetry between convex and concave body sides.
Liu [32]40 children and adolescents with AIS (age: 10–18 y)paravertebral muscles
Concave side: 18.27 kPa
Convex side: 14.31 kPa
No significant difference in muscle elasticity between the concave and the convex sides.
Pietton [35]16 children and adolescents with AIS (age: 13 ± 2.5 y); 19 healthy controls (age: 12.6 ± 1.7 y)ICMs
AIS: 2.2 ± 0.3 m/s
Healthy controls: 2.1 ± 0.4 m/s
SWE is feasible and reliable in the assessment of the ICMs of healthy individuals and those with scoliosis (ICC: 0.85 and 0.83, respectively).
Although the AIS group showed a tendency toward higher ICMs stiffness than in the healthy group, there was no significant difference between groups.

Table 5.

Studies using muscle shear-wave elastography in adolescent idiopathic scoliosis.

OE = external oblique muscle; OI = internal oblique muscle; TrA = transversus abdominis muscle; ICMs, intercostal muscles; kPa, kilopascal.

2.4 Congenital muscular torticollis

Congenital muscular torticollis (CMT) is a common muscular disorder occurring at or shortly after delivery as a result of the unilateral shortening of the sternocleidomastoid muscle (SCM), which results in clinical symptoms including head lateral tilt toward the ipsilateral side and head rotation to the opposite side [36, 37]. Long-lasting severe CMT can lead to asymmetric cranial and facial structures. Although the exact etiology of CMT remains unclear, endomysial fibrosis with collagen deposition and the migration of fibroblasts to individual muscle fibers are involved in the pathogenesis of CMT [38]. Ultimately, muscle fibrosis and increased stiffness can reduce the elasticity and function of the muscles, which leads to the range of motion deficit and contracture. Although CMT is a muscle-derived condition, the insufficient number of muscle SWE studies addressed the SCM stiffness indicates a large gap in the literature.

It was reported that the stiffness of the affected SCM was positively correlated with the degree of PROM deficit of neck rotation in the affected side [39, 40, 41] and affected SCM stiffness was significantly higher than that of the unaffected SCM and than that in the control group [39]. Hwang et al. also reported that SCM stiffness decreased significantly after 3 months of physiotherapy [41]. These studies point out the potential of muscle SWE in the diagnosis and treatment of CMT. Additional information on muscle SWE studies in CMT is provided in Table 6.

AuthorsParticipantsMuscle(s) and stiffness valuesFindings
Park [39]20 infants with CMT (age: 0.71 ± 0.25 mo); 12 healthy controls (age: 0.65 ± 0.27 mo)SCM
infants with CMT: 3.65 ± 0.75 m/s
Healthy controls: 1.50 ± 0.30 m/s
In the CMT group, the stiffness of the affected SCM was significantly higher than that of the unaffected SCM and than that in the control group.
The stiffness of the affected SCM was positively correlated with the degree of PROM deficit of neck rotation in the affected side (r = 0.77).
The intrarater reliability: ICC = 0.923.
Hwang [41]22 infants with CMT (age: 1.16 ± 0.66 mo)SCM
Initial assessment: 2.33 ± 0.47 m/s
After 3 months: 1.56 ± 0.63 m/s
The SCM stiffness decreased significantly from the initial evaluation to 3 months after the start of the physiotherapy.
The initial SCM stiffness showed negative correlations with the degree of cervical rotation and lateral flexion, respectively (r = −0.642 and r = −0.643)
Zhang [40]46 late-referral infants with CMT (age: 8.13 ± 1.77 mo)SCM
Affected SCM: 205.53 ± 46.34 kPa
Unaffected SCM: 27.91 ± 4.90 kPa
SCM stiffness was positively correlated with the degree of the PROM deficit in neck rotation (r = 0.82).
The intrarater reliability: ICC = 0.981

Table 6.

Studies using muscle shear-wave elastography in congenital muscular torticollis.

SCM, sternocleidomastoid muscle; PROM, passive range of motion; kPa, kilopascal.

2.5 Healthy children

Muscle SWE studies in healthy children are important for the reliability and repeatability of the measurement methods and to understand the effect of some individual factors such as sex and age on muscle stiffness. Brandenburg et al. reported that sex, age, BMI, extremity dominancy, and calf circumference were not associated with muscle stiffness in children [42]. Liu et al. compared the gastrocnemius medialis muscle stiffness of different age groups and found that there was no significant difference between sexes and muscle stiffness was the greatest in the older group, followed by the middle-aged group and then the children group [43]. Although these two studies give some clues, we think that further muscle SWE studies in healthy children are required and these studies are important especially for the measurement reliability, standardization of the measurement method, and establishing norm values for muscle stiffness. Additional information on muscle SWE studies in healthy children is provided in Table 7.

AuthorsParticipantsMuscle(s) and stiffness valuesFindings
Liu [43]27 children (age: 7.46 ± 1.46 y), 31
middle-aged individuals (age: 34.65 ± 3.19 y), and 28 older people
(age: 62.25 ± 2.72 y).
GM
Children: 24.28 ± 7.72 kPa
Middle-aged individuals: 28.39 ± 6.85 kPa
Older people: 34.89 ± 8.48 kPa
In all groups, passive muscle stiffness increased as the ankle DF increased.
There was no significant difference between sexes.
No significant difference in muscle stiffness between the three groups in terms of PF angles. The difference in muscle stiffness among the three groups became significant as DF increased.
In terms of the ankle angles of DF, the muscle stiffness was the greatest in the older group, followed by the middle-aged group and then the children group (that is, stiffness increases with age).
Brandenburg [42]20 healthy children (age range: 2–12 y),GL
R: 7.7 ± 2.5 kPa
L: 7.8 ± 3.3 kPa
Sex, age, BMI, extremity dominancy, and calf circumference did not significantly correlate with muscle stiffness.

Table 7.

Studies using muscle shear-wave elastography in healthy children.

GM, gastrocnemius medialis; GL, gastrocnemius lateralis; DF, dorsi flexion; PF, plantar flexion; BMI, body mass index; R, right; L, left; kPa, kilopascal.

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3. Conclusions

Muscle SWE is an exciting and rapidly evolving US technique that allows quantification of muscle stiffness with a non-invasive, non-painful, and non-irradiating examination. It has the potential of wider clinical use because it is relatively low-cost, it provides real-time measurement, it takes less time, especially for the pediatric population, and it is sedation/anesthesia-free. SWE shows promise as an adjunct clinical tool for differentiating between normal and abnormal muscles, monitoring the effectiveness of therapeutic interventions, altering the therapeutic intervention, or deciding treatment duration. Therefore, SWE, which measures individual muscle stiffness, can provide significant benefits, especially for physiotherapists because many rehabilitation strategies aim to change muscle structure. However, some remarkable points such as the insufficient number of studies, the small sample size, the differences in measurement settings and methods between studies, and the lack of norm values for different muscles indicate the necessity for further studies.

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Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.Bamber J, Cosgrove D, Dietrich CF, Fromageau J, Bojunga J, Calliada F, et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 1: Basic principles and technology. Ultraschall in der Medizin-European. Journal of Ultrasound. 2013;34(02):169-184
  2. 2.Brandenburg JE, Eby SF, Song P, Zhao H, Brault JS, Chen S, et al. Ultrasound elastography: The new frontier in direct measurement of muscle stiffness. Archives of Physical Medicine and Rehabilitation. 2014;95(11):2207-2219
  3. 3.Miller T, Ying M, Sau Lan Tsang C, Huang M, Pang MY. Reliability and validity of ultrasound elastography for evaluating muscle stiffness in neurological populations: A systematic review and meta-analysis. Physical Therapy. 2021;101(1):pzaa188
  4. 4.Goo M, Johnston LM, Hug F, Tucker K. Systematic review of instrumented measures of skeletal muscle mechanical properties: Evidence for the application of shear wave elastography with children. Ultrasound in Medicine & Biology. 2020;46(8):1831-1840
  5. 5.Mercuri E, Muntoni F. Muscular dystrophies. The Lancet. 2013;381(9869):845-860
  6. 6.Mendell JR, Shilling C, Leslie ND, Flanigan KM, al-Dahhak R, Gastier-Foster J, et al. Evidence-based path to newborn screening for Duchenne muscular dystrophy. Annals of Neurology. 2012;71(3):304-313
  7. 7.Desguerre I, Mayer M, Leturcq F, Barbet J-P, Gherardi RK, Christov C. Endomysial fibrosis in Duchenne muscular dystrophy: A marker of poor outcome associated with macrophage alternative activation. Journal of Neuropathology & Experimental Neurology. 2009;68(7):762-773
  8. 8.Mazzone E, Martinelli D, Berardinelli A, Messina S, D’Amico A, Vasco G, et al. North star ambulatory assessment, 6-minute walk test and timed items in ambulant boys with Duchenne muscular dystrophy. Neuromuscular Disorders. 2010;20(11):712-716
  9. 9.Stuberg WA, Metcalf W. Reliability of quantitative muscle testing in healthy children and in children with Duchenne muscular dystrophy using a hand-held dynamometer. Physical Therapy. 1988;68(6):977-982
  10. 10.Lin C-W, Tsui P-H, Lu C-H, Hung Y-H, Tsai M-R, Shieh J-Y, et al. Quantifying lower limb muscle stiffness as ambulation function declines in Duchenne muscular dystrophy with acoustic radiation force impulse shear wave elastography. Ultrasound in Medicine & Biology. 2021;47(10):2880-2889
  11. 11.Pichiecchio A, Alessandrino F, Bortolotto C, Cerica A, Rosti C, Raciti MV, et al. Muscle ultrasound elastography and MRI in preschool children with Duchenne muscular dystrophy. Neuromuscular Disorders. 2018;28(6):476-483
  12. 12.Lacourpaille L, Hug F, Guével A, Péréon Y, Magot A, Hogrel JY, et al. Non-invasive assessment of muscle stiffness in patients with Duchenne muscular dystrophy. Muscle & Nerve. 2015;51(2):284-286
  13. 13.Lacourpaille L, Gross R, Hug F, Guével A, Péréon Y, Magot A, et al. Effects of Duchenne muscular dystrophy on muscle stiffness and response to electrically-induced muscle contraction: A 12-month follow-up. Neuromuscular Disorders. 2017;27(3):214-220
  14. 14.Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, Damiano D, et al. A report: The definition and classification of cerebral palsy April 2006. Developmental Medicine and Child Neurology. Supplement. 2007;109(suppl. 109):8-14
  15. 15.Oskoui M, Coutinho F, Dykeman J, Jetté N, Pringsheim T. An update on the prevalence of cerebral palsy: A systematic review and meta-analysis. Developmental Medicine & Child Neurology. 2013;55(6):509-519
  16. 16.Brandenburg JE, Eby SF, Song P, Kingsley-Berg S, Bamlet W, Sieck GC, et al. Quantifying passive muscle stiffness in children with and without cerebral palsy using ultrasound shear wave elastography. Developmental Medicine & Child Neurology. 2016;58(12):1288-1294
  17. 17.Howard JJ, Graham K, Shortland AP. Understanding skeletal muscle in cerebral palsy: A path to personalized medicine? Developmental Medicine & Child Neurology. 2021. Sep 9. DOI: 10.1111/dmcn.15018. Epub ahead of print. PMID: 34499350
  18. 18.Smith LR, Lee KS, Ward SR, Chambers HG, Lieber RL. Hamstring contractures in children with spastic cerebral palsy result from a stiffer extracellular matrix and increased in vivo sarcomere length. The Journal of Physiology. 2011;589(10):2625-2639
  19. 19.Lallemant-Dudek P, Vergari C, Dubois G, Forin V, Vialle R, Skalli W. Ultrasound shearwave elastography to characterize muscles of healthy and cerebral palsy children. Scientific Reports. 2021;11(1):1-7
  20. 20.Vola E, Albano M, Di Luise C, Servodidio V, Sansone M, Russo S, et al. Use of ultrasound shear wave to measure muscle stiffness in children with cerebral palsy. Journal of Ultrasound. 2018;21(3):241-247
  21. 21.Bilgici MC, Bekci T, Ulus Y, Ozyurek H, Aydin OF, Tomak L, et al. Quantitative assessment of muscular stiffness in children with cerebral palsy using acoustic radiation force impulse (ARFI) ultrasound elastography. Journal of Medical Ultrasonics. 2018;45(2):295-300
  22. 22.Lee SS, Gaebler-Spira D, Zhang L-Q, Rymer WZ, Steele KM. Use of shear wave ultrasound elastography to quantify muscle properties in cerebral palsy. Clinical Biomechanics. 2016;31:20-28
  23. 23.Boulard C, Gautheron V, Lapole T. Mechanical properties of ankle joint and gastrocnemius muscle in spastic children with unilateral cerebral palsy measured with shear wave elastography. Journal of Biomechanics. 2021;124:110502. DOI: 10.1016/j.jbiomech.2021.110502. Epub 2021 Jun 7. PMID: 34126561
  24. 24.Bilgici MC, Bekci T, Ulus Y, Bilgici A, Tomak L, Selcuk MB. Quantitative assessment of muscle stiffness with acoustic radiation force impulse elastography after botulinum toxin A injection in children with cerebral palsy. Journal of Medical Ultrasonics. 2018;45(1):137-141
  25. 25.Dağ N, Cerit MN, Şendur HN, Zinnuroğlu M, Muşmal BN, Cindil E, et al. The utility of shear wave elastography in the evaluation of muscle stiffness in patients with cerebral palsy after botulinum toxin A injection. Journal of Medical Ultrasonics. 2020;47(4):609-615
  26. 26.Brandenburg JE, Eby SF, Song P, Bamlet W, Sieck GC, An K-N. Quantifying effect of onabotulinum toxin a on passive muscle stiffness in children with cerebral palsy using ultrasound shear wave elastography. American Journal of Physical Medicine & Rehabilitation. 2018;97(7):500
  27. 27.Bertan H, Oncu J, Vanli E, Alptekin K, Sahillioglu A, Kuran B, et al. Use of shear wave elastography for quantitative assessment of muscle stiffness after botulinum toxin injection in children with cerebral palsy. Journal of Ultrasound in Medicine. 2020;39(12):2327-2337
  28. 28.Doruk Analan P, Aslan H. Association between the elasticity of hip muscles and the hip migration index in cerebral palsy. Journal of Ultrasound in Medicine. 2019;38(10):2667-2672
  29. 29.Konieczny MR, Senyurt H, Krauspe R. Epidemiology of adolescent idiopathic scoliosis. Journal of Children’s Orthopaedics. 2013;7(1):3-9
  30. 30.Kouwenhoven J-WM, Castelein RM. The pathogenesis of adolescent idiopathic scoliosis: Review of the literature. Spine. 2008;33(26):2898-2908
  31. 31.Stokes I. Mechanical effects on skeletal growth. Journal of Musculoskeletal and Neuronal Interactions. 2002;2(3):277-280
  32. 32.Liu Y, Pan A, Hai Y, Li W, Yin L, Guo R. Asymmetric biomechanical characteristics of the paravertebral muscle in adolescent idiopathic scoliosis. Clinical Biomechanics. 2019;65:81-86
  33. 33.Linek P, Pałac M, Wolny T. Shear wave elastography of the lateral abdominal muscles in C-shaped idiopathic scoliosis: A case–control study. Scientific Reports. 2021;11(1):1-12
  34. 34.Linek P, Wolny T, Sikora D, Klepek A. Supersonic shear imaging for quantification of lateral abdominal muscle shear modulus in pediatric population with scoliosis: A reliability and agreement study. Ultrasound in Medicine & Biology. 2019;45(7):1551-1561
  35. 35.Pietton R, David M, Hisaund A, Langlais T, Skalli W, Vialle R, et al. Biomechanical evaluation of intercostal muscles in healthy children and adolescent idiopathic scoliosis: A preliminary study. Ultrasound in Medicine & Biology. 2021;47(1):51-57
  36. 36.Sargent B, Kaplan SL, Coulter C, Baker C. Congenital muscular torticollis: Bridging the gap between research and clinical practice. Pediatrics. 2019;144(2):e20190582
  37. 37.Ben Zvi I, Thompson DN. Torticollis in childhood—A practical guide for initial assessment. European Journal of Pediatrics. 2021;1–9. DOI: 10.1007/s00431-021-04316-4. Epub ahead of print. PMID: 34773160
  38. 38.Chen HX, Tang SP, Gao FT, et al. Fibrosis, adipogenesis, and muscle atrophy in congenital muscular torticollis. Medicine (Baltimore). 2014;93(23):e138. DOI: 10.1097/MD.0000000000000138
  39. 39.Park GY, Kwon DR, Kwon DG. Shear wave sonoelastography in infants with congenital muscular torticollis. Medicine. 2018;97(6):p e9818. DOI: 10.1097/MD.0000000000009818
  40. 40.Zhang C, Ban W, Jiang J, Zhou Q, Li J, Li M. Two-dimensional ultrasound and shear wave elastography in infants with late-referral congenital muscular torticollis. Journal of Ultrasound in Medicine. 2019;38(9):2407-2415
  41. 41.Hwang D, Shin YJ, Choi JY, Jung SJ, Yang S-S. Changes in muscle stiffness in infants with congenital muscular torticollis. Diagnostics. 2019;9(4):158
  42. 42.Brandenburg JE, Eby SF, Song P, Zhao H, Landry BW, Kingsley-Berg S, et al. Feasibility and reliability of quantifying passive muscle stiffness in young children by using shear wave ultrasound elastography. Journal of Ultrasound in Medicine. 2015;34(4):663-670
  43. 43.Liu X, Yu H-K, Sheng S-Y, Liang S-M, Lu H, Chen R-Y, et al. Quantitative evaluation of passive muscle stiffness by shear wave elastography in healthy individuals of different ages. European Radiology. 2021;31(5):3187-3194

Written By

Celik Halil Ibrahim and Karaduman Aynur Ayşe

Submitted: December 11th, 2021Reviewed: December 16th, 2021Published: January 16th, 2022